Marine Biology

, Volume 160, Issue 10, pp 2547–2560 | Cite as

Differential effect of ultraviolet exposure (UVR) in the stress response of the Dinophycea Gymnodinium sp. and the Chlorophyta Dunaliella tertiolecta: mortality versus survival

  • Josée Nina BouchardEmail author
  • Candela García-Gómez
  • M. Rosario Lorenzo
  • María SegoviaEmail author
Original Paper


Dunaliella tertiolecta (Chlorophyta) and Gymnodinium sp. (Dinophyceae) cells were exposed to ultraviolet radiation (UVR) (PAR, UVA and UVB: PAB) for 6 days either continuously or during a photoperiod. Both UVR treatments were harmful to Gymnodinium but exposure to continuous PAB had the most dramatic effects. Although a number of lesions/damage could have happened during the first few hours of exposure to UVR, in less than 24 h, Gymnodinium lost its ability to detoxify ROS efficiently, photoinhibition occurred, thymine dimers formed in the DNA, caspase-like enzymatic activities DEVDase sharply increased and cells died as determined by SYTOX-green staining. Superoxide dismutase activity did not significantly change with time, and although the catalase activity augmented in both treatments, cells still suffered from the UVR stress. Clearly, UVR was fatal to the dinoflagellate. For the chlorophyte, however, cell numbers increased regardless of the UVR treatment and mortality remained low (<20 %). F v/F m showed an initial decrease but then remained constant for both light treatments. After 6 days of continuous PAB exposure, however, signs of stress (thymine dimers, oxidative stress) paralleled a drop in catalase activity. Results obtained here demonstrate that the dinoflagellate Gymnodinium was much more sensitive and was harmed more rapidly by UVR exposure than the chlorophyte D. tertiolecta. The increased tolerance to UVR exposure of the chlorophyte may provide advantages over other more sensitive phytoplankton species within the photic zone. We provide strong support in the present study for repair being an important component of UV resistance in this species.


Reactive Oxygen Species Dinoflagellate Catalase Activity Light Treatment PSII Reaction Centre 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



The present work was supported by Research Grants CTM/MAR10-17216 from the Ministry for Science and Innovation (MICCIN) and P08-03800 from the Regional Science Research Programme (Junta de Andalucía) Spain to MS. JNB was funded to carry out a short-stay postdoctoral-grant at MS Laboratory by the Regional Science Research Programme (Junta de Andalucía, Spain). CG and MRL were funded by PhD grants associated to the Research Grants mentioned above. We are grateful to Patrick Neale for thorough discussions and suggestions.


  1. Andreasson KIM, Wängberg S-A (2006) Biological weighting functions as a tool for evaluating two ways to measure UVB radiation inhibition on photosynthesis. J Photochem Photobiol B 84:111–118CrossRefGoogle Scholar
  2. Andreasson KIM, Wängberg S-A (2007) Reduction in growth rate in Phaeodactylum tricornutum (Bacillariophyceae) and Dunaliella tertiolecta (Chlorophyceae) induced by UV-B radiation. J Photochem Photobiol B Biol 86:227–233CrossRefGoogle Scholar
  3. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399CrossRefGoogle Scholar
  4. Beardall J, Sobrino C, Stojkovic C (2009) Interactions between the impacts of ultraviolet radiation, elevated CO2, and nutrient limitation on marine primary producers. Photochem Photobiol Sci 8:1257CrossRefGoogle Scholar
  5. Boelen PI, Obernoster I, Vink A, Buma AGJ (1999) Attenuation of biologically effective UV radiation in tropical Atlantic waters measured with a biochemical DNA dosimeter. Photochem Photobiol 69:34–40CrossRefGoogle Scholar
  6. Bonneau L, Ge Y, Drury GE, Gallois P (2008) What happened to plant caspases? J Exp Bot 59:491–499CrossRefGoogle Scholar
  7. Bouchard JN, Purdie DA (2011a) Effect of elevated temperature, darkness, and hydrogen peroxide treatment on oxidative stress and cell death in the bloom-forming toxic cyanobacteria Microcystis aeruginosa. J Phycol 47:1316–1325CrossRefGoogle Scholar
  8. Bouchard JN, Purdie DA (2011b) Temporal variation of caspase 3-like protein activity in cultures of the harmful dinoflagellates Karenia brevis and Karenia mikimotoi. J Plankton Res 33:961–972CrossRefGoogle Scholar
  9. Bouchard JN, Campbell DA, Roy S (2005) Effects of ultraviolet-B radiation on the D1 protein repair cycle of natural phytoplankton communities from three latitudes (Canada, Brazil, Argentina). J Phycol 41:287–293CrossRefGoogle Scholar
  10. Bouchard JN, Roy S, Campbell DA (2006) UVB effects on the photosystem II-D1 protein of phytoplankton and natural phytoplankton communities. Photochem Photobiol 82:936–951CrossRefGoogle Scholar
  11. Buma AGJ, van Hannen EJ, Veldhuis MJW, Roza L, Gieskes WWC (1995) Monitoring UVB induced DNA damage in individual diatom cells by immunofluorescent thymine dimer detection. J Phycol 31:314–321CrossRefGoogle Scholar
  12. Buma AGJ, Boelen P, Jeffrey WH (2003) UVR-induced DNA damage in aquatic organisms. In: Helbling EW, Zagarese HE (eds) UV effects in aquatic organisms and ecosystems. Royal Society of Chemistry, Cambridge, pp 291–327Google Scholar
  13. Caldwell MM (1971) Solar UV irradiance and the growth and development oh higher plants. Photophysiology 4:131–177Google Scholar
  14. Cullen JJ, Neale PJ (1997) Biological weighting functions for describing the effects of ultraviolet radiation on aquatic systems. In: Hader D-P (ed) The effects of ozone depletion on aquatic ecosystems. R.G. Landes Company, Austin, pp 97–118Google Scholar
  15. Cullen JJ, Neale PJ, Lesser MP (1992) Biological weighting functions for describing the inhibition of phytoplankton photosynthesis by ultraviolet radiation. 258:646–650Google Scholar
  16. Darehshouri A, Affenzeller M, Lutz-Meindl U (2008) Cell death upon H2O2 induction in the unicellular green alga Micrasterias. Plant Biol 10:732–745CrossRefGoogle Scholar
  17. Davies KJA, Delsignore ME, Lin SW (1987) Protein damage and degradation by oxygen radicals. II. Modification of amino acids. J Biol Chem 262:9902–9907Google Scholar
  18. Foyer CH, Lelandais M, Kunert KJ (1994) Photooxidative stress in plants. Physiol Plantarum 92:696–717CrossRefGoogle Scholar
  19. Franklin DJ, Hoegh-Guldberg O, Jones RJ, Berges JA (2004) Cell death and degeneration in the symbiotic dinoflagellates of the coral Stylophora pistillata during bleaching. Mar Ecol Prog Ser 272:117–130CrossRefGoogle Scholar
  20. García-Gómez C, Parages ML, Jiménez C, Palma A, Mata MT, Segovia M (2012) Cell survival after UV stress in the unicellular chlorophyte Dunaliella tertiolecta is mediated by DNA repair and MAPKs phosphorylation. J Exp Bot 63(14):5259–5274CrossRefGoogle Scholar
  21. Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92CrossRefGoogle Scholar
  22. Gerber S, Häder DP (1995) Effects of artificial UVB and simulated solar radiation on the flagellate Euglena gracilis: physiological, spectroscopical and biochemical investigations. Acta Protozool 34:13–20Google Scholar
  23. Goldman JC, McCarthy JJ (1978) Steady state growth and ammonium uptake of a fast-growing marine diatom. Limnol Oceanogr 23:696–703CrossRefGoogle Scholar
  24. Guillard RRL, Ryther RH (1962) Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt and Detonula confervacea Cleve. Can J Microbiol 8:229–239CrossRefGoogle Scholar
  25. Helbling EW, Buma AGJ, Boer MK, Villafañe VE (2001) In situ impact of solar ultraviolet radiation on photosynthesis and DNA in temperate marine phytoplankton. Mar Ecol Prog Ser 211:43–49CrossRefGoogle Scholar
  26. Heraud P, Beardall J (2000) Changes in chlorophyll fluorescence during exposure of Dunaliella tertiolecta to UV radiation indicate a dynamic interaction between damage and repair processes. Photosynth Res 63:123–134CrossRefGoogle Scholar
  27. Jahnke LS, White AL (2003) Long-term hyposaline and hypersaline stresses produce distinct antioxidant responses in the marine alga Dunaliella tertiolecta. J Plant Physiol 160:1193–1202CrossRefGoogle Scholar
  28. Janknegt PJ, de Graaff CM, van de Poll WH, Visser RJW, Helbling EW, Buma AGJ (2009) Antioxidative responses of two marine microalgae during acclimation to static and fluctuating natural UVR. Photochem Photobiol 85:1336–1345CrossRefGoogle Scholar
  29. Jiménez C, Capasso JM, Edelstein CL, Rivard CJ, Lucia S, Breusegem S, Berl T, Segovia M (2009) Different ways to die: cell death modes of the unicellular chlorophyte Dunaliella viridis exposed to various environmental stresses are mediated by the caspase-like activity DEVDase. J Exp Bot 60:815–828CrossRefGoogle Scholar
  30. Jones LW, Kok B (1966) Photoinhibition of chloroplast reactions. I. Kinetics and action spectra. Plant Physiol 41:1037–1043CrossRefGoogle Scholar
  31. Klisch M, Häder DP (2002) Mycosporine-like amino acids in the marine dinoflagellate Gyrodinium dorsum: induction by ultraviolet irradiation. J Photochem Photobiol, B 55:178–182CrossRefGoogle Scholar
  32. Korbee N, Mata MT, Figueroa FL (2010) Photoprotection mechanisms against ultraviolet radiation in Heterocapsa sp. (Dinophyceae) are influenced by nitrogen availability: mycosporine-like amino acids vs. xanthophyll cycle. Limnol Oceanogr 55:899–908CrossRefGoogle Scholar
  33. Lesser MP (1996) Acclimation of phytoplankton to UVB radiation: oxidative stress and photoinhibition of photosynthesis are not prevented by UVA absorbing compounds in the dinoflagellate Prorocentrum micans. Mar Ecol Prog Ser 132:287–297CrossRefGoogle Scholar
  34. Lesser MP (1997) Oxidative stress causes coral bleaching during exposure to elevated temperatures. Coral Reefs 16:187–192CrossRefGoogle Scholar
  35. Lesser MP (2006) Oxidative stress in marine environments: biochemistry and physiological ecology. Annu Rev Physiol 68:253–278CrossRefGoogle Scholar
  36. Lesser MP (2012) Oxidative stress in tropical marine ecosystems. In: Abele D, Vázquez-Medina JP, Zenteno-Savín T (eds) Oxidative stress in tropical marine ecosystems. Blackwell, Hoboken, pp 9–19Google Scholar
  37. Litchman E, Neale PJ, Banaszak AT (2002) Increased sensitivity to ultraviolet radiation in nitrogen-limited dinoflagellates: photoprotection and repair. Limnol Oceanogr 47:86–94CrossRefGoogle Scholar
  38. Llabrés M, Agustí S (2010) Effects of ultraviolet radiation on growth, cell death and the standing stock of Antarctic phytoplankton. Aquat Microb Ecol 59:151–160CrossRefGoogle Scholar
  39. McCord JM, Fridovich I (1969) Superoxide dismutase: an enzymic function for erythrocuprein (hemocuprein). J Biol Chem 244:6049–6055Google Scholar
  40. Moharikar S, D’Souza JS, Kulkarni AB, Rao B (2006) Apoptotic-like cell death pathway is induced in unicellular chlorophyte Chlamydomonas reinhardtii (chlorophyceae) cells following UV irradiation: detection and functional analyses. J Phycol 42:423–433CrossRefGoogle Scholar
  41. Neale PJ, Kieber DJ (2000) Assessing biological and chemical effects of UV in the marine environment: spectral weighting functions. Issues in environmental science and technology 14:61–83Google Scholar
  42. Neale PJ, Banaszak AT, Jarriel CR (1998a) Ultraviolet sunscreens in Gymnodinium sanguineum (Dinophyceae): mycosporine-like amino acids protect again inhibition of photosynthesis. J Phycol 34:928–938CrossRefGoogle Scholar
  43. Neale PJ, Davis RF, Cullen JJ (1998b) Interactive effects of ozone depletion and vertical mixing on photosynthesis of Antarctic phytoplankton. Nature 392:585–589CrossRefGoogle Scholar
  44. Pryor WA (1986) Oxy-radicals and related species: their formation, lifetimes, and reactions. Annu Rev Physiol 48:657–667CrossRefGoogle Scholar
  45. Rijstenbil JW, Derksen JWM, Gerringa LJA, Poortvliet TCW, Sandee A, Van den Berg M, Van Drie J, Wijnholds JA (1994) Oxidative stress induced by copper: defense and damage in the marine planktonic diatom Ditylum brightwellii (Grunow), grown in continuous cultures with high and low zinc levels. Mar Biol 119:583–590CrossRefGoogle Scholar
  46. Roy S (2000) Strategies for the minimisation of the UV-induced damage. In: de Mora SJ, Demers S, Vernet M (eds) The effects of UV radiation in the marine environment. Cambridge University Press, Cambridge, pp 177–205CrossRefGoogle Scholar
  47. Rozema J, Blokker P, Mayoral Fuertes MA, Broekman R (2009) UV-B absorbing compounds in present-day and fossil pollen, spores, cuticles, seed coats and wood: evaluation of a proxy for solar UV radiation. Photochem Photobiol Sci 8:1233CrossRefGoogle Scholar
  48. Schreiber U, Bilger W, Schliwa U (1986) Continuous recording of photochemical and non-photochemical quenching with a new type of modulation fluorometer. Photosynth Res 10:51–62CrossRefGoogle Scholar
  49. Segovia M (2008) Programmed cell death in dinoflagellates. In: Pérez Martin JM (ed) Programmed cell death in protozoa. Landes Bioscience. Austin, pp 126–142Google Scholar
  50. Segovia M, Berges JA (2005) Effects of inhibitors of protein synthesis and DNA replication on the induction of proteolytic activities, caspase-like activities and cell death in the unicellular chlorophyte Dunaliella tertiolecta. Eur J Phycol 40:21–30CrossRefGoogle Scholar
  51. Segovia M, Berges JA (2009) Inhibition of caspase-like activities prevents the appearance of reactive oxygen species and dark-induced apoptosis in the unicellular chlorophyte Dunaliella tertiolecta. J Phycol 45:1116–1126CrossRefGoogle Scholar
  52. Segovia M, Haramaty L, Berges JA, Falkowski PG (2003) Cell death in the unicellular chlorophyte Dunaliella tertiolecta. A hypothesis on the evolution of apoptosis in higher plants and metazoans. Plant Physiol 132:99–105CrossRefGoogle Scholar
  53. Setlow RB (1974) The wavelengths in sunlight effective in producing skin cancer: a theoretical analysis. PNAS 71:3363–3366CrossRefGoogle Scholar
  54. Sinha RP, Häder D-P (2002) UV-induced DNA damage and repair: a review. Photochem Photobiol Sci 1:225–236CrossRefGoogle Scholar
  55. Tang H, Abunasser N, Garcia MED, Chen M, Simon KY, Salley SO (2011) Potential of microalgae oil from Dunaliella tertiolecta as a feedstock for biodiesel. Appl Energ 88:3324–3330CrossRefGoogle Scholar
  56. Tian J, Yu J (2009) Changes in ultrastructure and responses of antioxidant systems of algae (Dunaliella salina) during acclimation to enhanced ultraviolet-B radiation. J Photochem Photobiol, B 97:152–160CrossRefGoogle Scholar
  57. Tsiatsiani L, Van Breusegem F, Gallois P, Zavialov A, Lam E, Bozhkov PV (2011) Metacaspases. Cell Death Differ 18:1279–1288CrossRefGoogle Scholar
  58. Van de Poll WH, Alderkamp AC, Janknegt PJ, Roggeveld J, Buma AGJ (2006) Photoacclimation modulates excessive photosynthetically active and ultraviolet radiation effects in a temperate and Antarctic marine diatom. Limnol Oceanogr 51:1239–1248CrossRefGoogle Scholar
  59. Vartapetian AB, Tuzhikov AI, Chichkova NV, Taliansky M, Wolpert TJ (2011) A plant alternative to animal caspases: subtilisin-like proteases. Cell Death Differ 18:1289–1297CrossRefGoogle Scholar
  60. Veldhuis MJW, Kraay GW, Timmermans KR (2001) Cell death in phytoplankton: correlation between changes in membrane permeability, photosynthetic activity, pigmentation and growth. Eur J Phycol 36:167–177CrossRefGoogle Scholar
  61. Vernet M (2000) Effects of UV radiation on the physiology and ecology of marine phytoplankton. In: de Mora SJ, Demers S, Vernet M (eds) The effects of UV radiation in the marine environment. Cambridge University Press, Cambridge, pp 237–278CrossRefGoogle Scholar
  62. Villafañe VE, Sundbäck K, Figueroa FL, Helbling EW (2003) Photosynthesis in the aquatic environment as affected by UVR. In: Helbling EW, Zagarese HE (eds) UV effects in aquatic organisms and ecosystems. Royal Society of Chemistry, Cambridge, pp 357–397Google Scholar
  63. Vincent WF, Roy S (1993) Solar ultraviolet-B radiation and aquatic primary production: damage, protection and recovery. Environ Rev 1:1–12CrossRefGoogle Scholar
  64. Winterbourn CC (2008) Reconciling the chemistry and biology of reactive oxygen species. Nat Chem Biol 4:278–286CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.National Oceanography CentreUniversity of SouthamptonSouthamptonUK
  2. 2.Department of Ecology, Faculty of SciencesUniversity of MálagaMálagaSpain
  3. 3.Algenol BiofuelsFort MyersUSA

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